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Uncovering the molecular mechanisms of lignocellulose digestion in shipworms

Lignocellulose forms the structural framework of woody plant biomass and represents the most abundant carbon source in the biosphere. Turnover of woody biomass is a critical component of the global carbon cycle, and the enzymes involved are of increasing industrial importance as industry moves away...

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Autores principales: Sabbadin, Federico, Pesante, Giovanna, Elias, Luisa, Besser, Katrin, Li, Yi, Steele-King, Clare, Stark, Meg, Rathbone, Deborah A., Dowle, Adam A., Bates, Rachel, Shipway, J. Reuben, Cragg, Simon M., Bruce, Neil C., McQueen-Mason, Simon J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5840672/
https://www.ncbi.nlm.nih.gov/pubmed/29527236
http://dx.doi.org/10.1186/s13068-018-1058-3
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author Sabbadin, Federico
Pesante, Giovanna
Elias, Luisa
Besser, Katrin
Li, Yi
Steele-King, Clare
Stark, Meg
Rathbone, Deborah A.
Dowle, Adam A.
Bates, Rachel
Shipway, J. Reuben
Cragg, Simon M.
Bruce, Neil C.
McQueen-Mason, Simon J.
author_facet Sabbadin, Federico
Pesante, Giovanna
Elias, Luisa
Besser, Katrin
Li, Yi
Steele-King, Clare
Stark, Meg
Rathbone, Deborah A.
Dowle, Adam A.
Bates, Rachel
Shipway, J. Reuben
Cragg, Simon M.
Bruce, Neil C.
McQueen-Mason, Simon J.
author_sort Sabbadin, Federico
collection PubMed
description Lignocellulose forms the structural framework of woody plant biomass and represents the most abundant carbon source in the biosphere. Turnover of woody biomass is a critical component of the global carbon cycle, and the enzymes involved are of increasing industrial importance as industry moves away from fossil fuels to renewable carbon resources. Shipworms are marine bivalve molluscs that digest wood and play a key role in global carbon cycling by processing plant biomass in the oceans. Previous studies suggest that wood digestion in shipworms is dominated by enzymes produced by endosymbiotic bacteria found in the animal’s gills, while little is known about the identity and function of endogenous enzymes produced by shipworms. Using a combination of meta-transcriptomic, proteomic, imaging and biochemical analyses, we reveal a complex digestive system dominated by uncharacterized enzymes that are secreted by a specialized digestive gland and that accumulate in the cecum, where wood digestion occurs. Using a combination of transcriptomics, proteomics, and microscopy, we show that the digestive proteome of the shipworm Lyrodus pedicellatus is mostly composed of enzymes produced by the animal itself, with a small but significant contribution from symbiotic bacteria. The digestive proteome is dominated by a novel 300 kDa multi-domain glycoside hydrolase that functions in the hydrolysis of β-1,4-glucans, the most abundant polymers in wood. These studies allow an unprecedented level of insight into an unusual and ecologically important process for wood recycling in the marine environment, and open up new biotechnological opportunities in the mobilization of sugars from lignocellulosic biomass. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-018-1058-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-58406722018-03-09 Uncovering the molecular mechanisms of lignocellulose digestion in shipworms Sabbadin, Federico Pesante, Giovanna Elias, Luisa Besser, Katrin Li, Yi Steele-King, Clare Stark, Meg Rathbone, Deborah A. Dowle, Adam A. Bates, Rachel Shipway, J. Reuben Cragg, Simon M. Bruce, Neil C. McQueen-Mason, Simon J. Biotechnol Biofuels Research Lignocellulose forms the structural framework of woody plant biomass and represents the most abundant carbon source in the biosphere. Turnover of woody biomass is a critical component of the global carbon cycle, and the enzymes involved are of increasing industrial importance as industry moves away from fossil fuels to renewable carbon resources. Shipworms are marine bivalve molluscs that digest wood and play a key role in global carbon cycling by processing plant biomass in the oceans. Previous studies suggest that wood digestion in shipworms is dominated by enzymes produced by endosymbiotic bacteria found in the animal’s gills, while little is known about the identity and function of endogenous enzymes produced by shipworms. Using a combination of meta-transcriptomic, proteomic, imaging and biochemical analyses, we reveal a complex digestive system dominated by uncharacterized enzymes that are secreted by a specialized digestive gland and that accumulate in the cecum, where wood digestion occurs. Using a combination of transcriptomics, proteomics, and microscopy, we show that the digestive proteome of the shipworm Lyrodus pedicellatus is mostly composed of enzymes produced by the animal itself, with a small but significant contribution from symbiotic bacteria. The digestive proteome is dominated by a novel 300 kDa multi-domain glycoside hydrolase that functions in the hydrolysis of β-1,4-glucans, the most abundant polymers in wood. These studies allow an unprecedented level of insight into an unusual and ecologically important process for wood recycling in the marine environment, and open up new biotechnological opportunities in the mobilization of sugars from lignocellulosic biomass. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-018-1058-3) contains supplementary material, which is available to authorized users. BioMed Central 2018-03-07 /pmc/articles/PMC5840672/ /pubmed/29527236 http://dx.doi.org/10.1186/s13068-018-1058-3 Text en © The Author(s) 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Sabbadin, Federico
Pesante, Giovanna
Elias, Luisa
Besser, Katrin
Li, Yi
Steele-King, Clare
Stark, Meg
Rathbone, Deborah A.
Dowle, Adam A.
Bates, Rachel
Shipway, J. Reuben
Cragg, Simon M.
Bruce, Neil C.
McQueen-Mason, Simon J.
Uncovering the molecular mechanisms of lignocellulose digestion in shipworms
title Uncovering the molecular mechanisms of lignocellulose digestion in shipworms
title_full Uncovering the molecular mechanisms of lignocellulose digestion in shipworms
title_fullStr Uncovering the molecular mechanisms of lignocellulose digestion in shipworms
title_full_unstemmed Uncovering the molecular mechanisms of lignocellulose digestion in shipworms
title_short Uncovering the molecular mechanisms of lignocellulose digestion in shipworms
title_sort uncovering the molecular mechanisms of lignocellulose digestion in shipworms
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5840672/
https://www.ncbi.nlm.nih.gov/pubmed/29527236
http://dx.doi.org/10.1186/s13068-018-1058-3
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